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Zoonotic Abbreviata Caucasica in Wild Chimpanzees (Pan Troglodytes Verus) from Senegal

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Zoonotic Abbreviata Caucasica in Wild Chimpanzees (Pan Troglodytes Verus) from Senegal pathogens Article Zoonotic Abbreviata caucasica in Wild Chimpanzees (Pan troglodytes verus) from Senegal Younes Laidoudi 1,2 , Hacène Medkour 1,2 , Maria Stefania Latrofa 3, Bernard Davoust 1,2, Georges Diatta 2,4,5, Cheikh Sokhna 2,4,5, Amanda Barciela 6 , R. Adriana Hernandez-Aguilar 6,7 , Didier Raoult 1,2, Domenico Otranto 3 and Oleg Mediannikov 1,2,* 1 IRD, AP-HM, Microbes, Evolution, Phylogeny and Infection (MEPHI), IHU Méditerranée Infection, Aix Marseille Univ, 19-21, Bd Jean Moulin, 13005 Marseille, France; [email protected] (Y.L.); [email protected] (H.M.); [email protected] (B.D.); [email protected] (D.R.) 2 IHU Méditerranée Infection, 19-21, Bd Jean Moulin, 13005 Marseille, France; [email protected] (G.D.); [email protected] (C.S.) 3 Department of Veterinary Medicine, University of Bari, 70010 Valenzano, Italy; [email protected] (M.S.L.); [email protected] (D.O.) 4 IRD, SSA, APHM, VITROME, IHU Méditerranée Infection, Aix-Marseille University, 19-21, Bd Jean Moulin, 13005 Marseille, France 5 VITROME, IRD 257, Campus International UCAD-IRD, Hann, Dakar, Senegal 6 Jane Goodall Institute Spain and Senegal, Dindefelo Biological Station, Dindefelo, Kedougou, Senegal; [email protected] (A.B.); [email protected] (R.A.H.-A.) 7 Department of Social Psychology and Quantitative Psychology, Faculty of Psychology, University of Barcelona, Passeig de la Vall d’Hebron 171, 08035 Barcelona, Spain * Correspondence: [email protected]; Tel.: +33-041-373-2401 Received: 19 April 2020; Accepted: 23 June 2020; Published: 27 June 2020 Abstract: Abbreviata caucasica (syn. Physaloptera mordens) has been reported in human and various non-human primates including great apes. The identification of this nematode is seldom performed and relies on egg characterization at the coproscopy, in the absence of any molecular tool. Following the recovery of two adult females of A. caucasica from the feces of wild Senegalese chimpanzees, morphometric characteristics were reported and new data on the width of the esophagus (0.268–0.287 mm) and on the cuticle structure (0.70–0.122 mm) were provided. The molecular characterization of a set of mitochondrial (cox1, 16S rRNA, 12S rRNA) and nuclear (18S rRNA and ITS2) partial genes was performed. Our phylogenetic analysis indicates for the first time that A. caucasica is monophyletic with Physaloptera species. A novel molecular tool was developed for the routine diagnosis of A. caucasica and the surveillance of Nematoda infestations. An A. caucasica-specific qPCR targeting the 12S gene was assessed. The assay was able to detect up to 1.13 10 3 eggs/g × − of fecal matter irrespective of its consistency, with an efficiency of 101.8% and a perfect adjustment (R2 = 0.99). The infection rate by A. caucasica in the chimpanzee fecal samples was 52.08%. Only 6.19% of the environmental samples were positive for nematode DNA and any for A. caucasica. Our findings indicate the need for further studies to clarify the epidemiology, circulation, life cycle, and possible pathological effects of this infestation using the molecular tool herein developed. Keywords: Abbreviata caucasica; Physaloptera mordens; Pan troglodytes verus; wild chimpanzees; nematode; zoonosis; Senegal 1. Introduction Physalopteriasis is caused by parasitic nematodes from the genus Physaloptera (Spirurida, Physalopteridae) [1], which has been distributed in Africa and the Middle East (i.e., Iran) since Pathogens 2020, 9, 517; doi:10.3390/pathogens9070517 www.mdpi.com/journal/pathogens Pathogens 2020, 9, 517 2 of 22 prehistoric times [2,3]. Following the first formal description of the Physaloptera genus (Rudolphi in 1819), Physaloptera abbreviata (Rudolphi, 1819) was designated as the type species [4]. Afterward, Abbreviata was defined as a distinct genus, based on the number, mode, and origin of the uteri, which constitute the main keys for genus differentiation [4]. Adult stages of this genus are found in the stomach of a variety of animals such as reptiles and mammals including humans [5]. Abbreviata (=Physaloptera) caucasica (Linstow 1902), is a gastrointestinal nematode of Simiiformes (Anthropoidea) members [6]. After its discovery in a Caucasian man, Linstow (1902) provided an incomplete description with some erroneous morphological details [7]. In 1926, Schulz gave the complete description of A. caucasica after re-examining the original specimens, establishing a close relationship of this species with Physaloptera mordens (Leiper, 1908) isolated from humans in Central Africa. The unique difference identified among specimens was the presence/absence of a series of small teeth between and exterior to the large teeth on the inner face of the lip of A. caucasica and P. mordens, respectively [8]. A few months later, Ortlepp re-examined P. mordens and confirmed that the small teeth were missing in the previous examinations [9], therefore synonymizing P. mordens (Leiper, 1908) and A. caucasica (Linstow, 1902). The A. caucasica infection has been reported in New and Old World monkeys [10], rhesus macaques (Macaca mulatta), baboons (Papio spp.), and great apes including both captive (Pongo spp.) and wild (Pongo abelii)[1,11]. It has also been reported in chimpanzees (Pan troglodytes) from Gombe (Tanzania) and Ngogo (Uganda) [12,13], although no adult specimens were examined. Furthermore, eggs of Physaloptera sp. have been reported in wild Senegalese chimpanzees [12,14]. Human and non-human primates probably constitute the natural host for A. caucasica [8]. The adult parasite looks like Ascaris sp. under the naked eye [15] and occurs in the digestive tract from the esophagus to the small intestine, where it can induce serious disease manifestations such as abdominal pain, anorexia, vomiting, and bloody diarrhea [2]. Records of the clinical signs in infected chimpanzees are lacking [6]. Nowadays, the detection of A. caucasica depends on the identification of eggs in the feces or in the detection of adult stages during post-mortem examination of the gastrointestinal tract of infested hosts [1]. The arthropod intermediate and/or paratenic hosts remain unknown though some experimental evidence indicates that A. caucasica could develop to the infective stage in Blatella germanica and in Schistocerca gregaria [5]. For other Physaloptera species, the intermediate arthropod host has been assessed such as Tribolium confusum [16], ground beetles, Harpalus sp. [17] as well as crickets, Acheta assimilis, and grasshoppers, Melanoplus femurrubrum [18,19]. Under natural conditions, A. caucasica may develop in arthropods and infestation probably occurs through ingestion of beetles, crickets, or other arthropods as well as paratenic hosts containing infective larvae [8,15]. However, the potential involvement of up to 28 paratenic and second intermediate hosts is suspected [6]. Anthelminthic drugs have been reported to be effective for the treatment of physalopteriasis in non-human primates [1]. However, their control should be reinforced by a molecular characterization to avoid the misleading conclusions about this parasite, sanitation and control of the potential paratenic or arthropod hosts as well as the surveillance of the infestation from the colon of non-human primates [1,16]. As part of the control of infectious and zoonotic diseases in the current chimpanzee population from the Dindefelo Community Natural Reserve in Senegal, we present here morphometric and phylogenetic findings to support the occurrence of A. caucasica in chimpanzees, providing a molecular characterization of a set of target mitochondrial (cox1, 16S rRNA, 12S rRNA) and nuclear (18S rRNA and ITS2) genes and morphological identification of adult specimens collected from feces of West African chimpanzees in Senegal. In addition, we developed a molecular test that could be used in a routine diagnostic laboratory instead of the labor-intensive coprological methods. The molecular test provides detection, egg quantification, and genetic characterization of A. caucasica from biological samples. We therefore applied this tool to a surveillance process and molecular xenomonitoring of A. caucasica from possible intermediate hosts and our current population of West African chimpanzees from Senegal. Pathogens 2020, 9, 517 3 of 22 2. Results 2.1. Morphological Characteristics of Adult A. caucasica Comparative measurements of A. caucasica adult females from our study with A. caucasica (Linstow, 1902) and its synonymous species P. mordens (Lipper, 1908) [8] are detailed in Table1. Two female complete specimens measuring 54.7 mm and 59.6 mm in length and 2.08 mm and 2.13 mm in width, respectively, were examined. The nematodes were characterized by the anterior end with a short buccal cavity (Figure1(1a)) and by a cuticle reflecting over the lips to form a cephalic collarette (Figure1(1b)) with two lateral pseudolabia undivided (Figure1(1c,1d)). Nerve ring at 0.430 mm from the anterior end. The esophagus consisting of two parts: muscular esophagus 0.75 mm long (Figure1(2a)) and 0.287 mm wide, 0.79 mm long, and 0.268 mm wide, respectively. The esophagus total length was 5.52 mm and 4.82 mm, respectively in two samples. In the mid-body, the cuticle was 0.70–0.122 mm thick and finely striated (Figure1(2b)). The worms showed the presence of two small symmetrical pins in the front third of the body (Figure1(2c)). Vulva 1.560 mm from anterior end (Figure1(2d)). Presence of four uteri (Figure1(3a)). Eggs were small 36–41 µm 28–32 µm (Figure1(3b)). Tail length was 1.084 mm (Figure1(3c)). The caudal end showed the × presence of a caudal appendix (Figure1(3d)). Pathogens 2020, 9, 517 4 of 22 Table 1. Comparative measurement (in mm unless specified) of adult female of A. caucasica from our study with A. caucasica (Linstow, 1902) and its synonymous species P. mordens (Lipper, 1908) according to Fain and Vandepitte (1964) [7], Linstow (1902) and Schulz (1926) [8]. Measurement of Fain and Measurement of This Study Measurement of Schulz (1926) Vandepitte (1964) Linstow, 1902 A. caucasica (Syn. P. A. caucasica: Measures A.
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